THIEME

8 Original Article

Ocular Affection as an Extraintestinal

Manifestation in Cases of Inflammatory Bowel
Disease at the Kafrelsheikh Governorate
Afecção ocular como manifestação extraintestinal em
casos de doença inflamatória intestinal
Mohammed Hussien Ahmed1 Mohammed Elashery2 Hebatallah Abdel Maksoud3
Aya Mohammed Mahros1

1 Department of Hepatology, Gastroenterology and Infectious
Diseases, Faculty of Medicine, Kafrelsheikh University, Kafr Al Sheikh
First, Kafr El Sheikh Governorate, Egypt
2 Department of Ophthalmology, Faculty of Medicine, Kafrelsheikh
University, Kafr Al Sheikh First, Kafr El Sheikh Governorate, Egypt
3 Department of Community Medicine, Faculty of Medicine,
Kafrelsheikh University, Kafr Al Sheikh First, Kafr El Sheikh
Governorate, Egypt
Address for correspondence Aya Mohammed Mahros, MD,
Department of Hepatology, Gastroenterology and Infectious
Diseases, Faculty of Medicine, Kafrelsheikh University, Kafr Al Sheikh
First, Kafr El Sheikh Governorate, Egypt
(e-mail: yoye_85@hotmail.com).

J Coloproctol 2021;41(1):8–13.

Abstract Introduction The manifestations of inflammatory bowel disease (IBD) are not
restricted to the gastrointestinal tract. Musculoskeletal conditions are considered
the most common extraintestinal manifestations, followed by mucocutaneous and
ocular diseases. Many general practitioners are unaware of the variety and severity of
the ocular affection in IBD patients.
Objective To assess the prevalence of extraintestinal manifestations in IBD patients at
Kafrelsheikh governorate, and to evaluate the different ocular manifestations and their
relationship to the severity of the disease.
Methods A cross-sectional study evaluating 120 patients treated at the Kafrelsheikh
University Hospital. The diagnosis of IBD was made between December 2018 and
December 2019 through clinical, endoscopic and histopathological examinations. All
patients were assessed for any extraintestinal manifestation or evidence of ocular
affection through slit-lamp examinations, tonometry, visual acuity, and indirect
ophthalmoscopy.
Keywords Results The mean age of the sample was 35.5
13.3 years. In total, 52 (43.3%)
► inflammatory bowel patients were male and 68 (56.7%) were female. Ocular manifestations represent 
disease 22.5% of extraintestinal manifestations. The most common ocular findings were
► ocular manifestations conjunctivitis (25.8%) and anterior uveitis (10.8%), followed by scleritis (9.2%) and

received DOI https://doi.org/ © 2021. Sociedade Brasileira de Coloproctologia. All rights

April 7, 2020 10.1055/s-0041-1724056. reserved.
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 Ocular Affectation in cases of IBD Ahmed et al. 9

cataract (8.3%). Other extraintestinal manifestations were observed in 41 (34.1%) 29

(29.9%) of ulcerative colitis cases, and 12 (52%) of Crohn disease cases. There was no
statistically significant difference in the presence of ocular involvement in relation to
the two types of IBD included in the Montreal classification.
Conclusion Ocular manifestations in cases of IBD are common and usually nonspe-
cific in presentation. The severity of the IBD does not reflect the severity of the ocular
affection.

Resumo Introdução As manifestações da doença inflamatória intestinal (DII) não se restrin-

gem ao trato gastrointestinal. Distúrbios musculoesqueléticos são considerados as
manifestações extraintestinais mais comuns, seguidos de doenças oculares e muco-
cutâneas. Muitos clínicos gerais desconhecem a variedade e a severidade das afecções
oculares em casos de DII.
Objetivo Determinar a prevalência das manifestações extraintestinais em pacientes
com DII na província de Kafrelsheikh, no Egito, e avaliar as diferentes manifestações
oculares e sua relação com a gravidade da doença.
Métodos Um estudo transversal que avaliou 120 pacientes tratados no Kafrelsheikh
University Hospital. O diagnóstico de DII foi feito entre dezembro de 2018 e dezembro
de 2019 por meio de exames clínicos, endoscópicos e histopatológicos. Por meio de
exames de lâmpada de fenda, tonometria, acuidade visual, e oftalmoscopia indireta,
todos os pacientes foram avaliados para se determinar a ocorrência de quaisquer
manifestações extraintestinais ou afecções oculares.
Resultados A média de idade da amostra foi de 35,5
13,3 anos. No total, 52 (43,3%)
pacientes com DII eram do sexo masculino, e 68 (56,7%), do sexo feminino. As
manifestações oculares representaram  22,5% das manifestações extraintestinais. Os
achados oculares mais comuns foram conjuntivite (25,8%) e uveíte anterior (10,8%),
seguidas de esclerite (9,2%) e catarata (8,3%). Outras manifestações extraintestinais
foram observadas em 41 (34,1%) pacientes, entre elas, 29,9% de casos de colite
ulcerativa, e 52% de casos de doença de Crohn. Não houve diferença estatisticamente
Palavras-chave significativa na presença de envolvimento ocular com relação aos dois tipos de DII
► doença inflamatória descritos na classificação de Montreal.
intestinal Conclusão As manifestações oculares em pacientes de DII são comuns e, geralmente,
► manifestações não específicas em termos de apresentação. A gravidade da DII não reflete a gravidade
oculares da afecção ocular.

Introduction inflammatory origin,4,5 and they are classified into

The manifestations of the two types of inflammatory bowel
disease (IBD), Crohn disease and ulcerative colitis, are not
restricted to the gastrointestinal tract. Unfortunately, the
patients may develop various extraintestinal manifestations
(EIMs),1 whose onset may be at any time during the course
of the disease, and musculoskeletal conditions are consid-
ered one of the most common, followed by mucocutaneous
and ophthalmic diseases.2,3 But other organs, such as the
skin, the liver, and the kidney, as well as the endocrine
systems, can be involved, leading to significant morbidity
and representing a challenge to the clinicians who manage
those patients. In fact, many general practitioners are
unaware of the variety and severity of ocular affections in
cases of IBD. These ocular complications are usually of an
primary, secondary, and coincidental. Primary complica-
tions are temporally related to IBD exacerbations, and
usually respond to anti-inflammatory drugs. These include
keratopathy, episcleritis, and scleritis. Secondary complica-
tions, such as scleromalacia due to scleritis, and dry eye due
to hypovitaminosis A following gut resection, occur as a
result of the primary complications. Coincidental compli-
cations commonly occur in the general population, and
cannot be correlated to IBD alone. These include conjuncti-
vitis, recurrent corneal ulcer, and corneal erosions.6The goal
of the present prospective randomized clinical study was to
assess the prevalence of EIMs among IBD patients at the
Kafrelsheikh governorate, and to evaluate the different
ocular affections and their relationship to the severity of
the disease.

J Coloproctol Vol. 41 No. 1/2021 © 2021. Sociedade Brasileira de Coloproctologia. All rights reserved.
10 Ocular Affectation in cases of IBD Ahmed et al.

variables were prescribed using number and percent, Chi-

Patients and Methods
Participants
The present is a cross-sectional study performed on 120
patients who had been previously diagnosed with IBD at the
Kafrelsheikh University Hospital from December 2018 to
December 2019. We included patients previously diagnosed
with IBD by endoscopy and histopathological examinations,
and excluded patients with previous chronic eye disease that
was not related to IBD, as well as those who refused the
follow-up evaluation.
Baseline Evaluation
All patients were required to provide a detailed medical
history, and they underwent a complete clinical examination
for any EIMs (especially ocular manifestations), associated
autoimmune diseases, and endocrinological diseases or evi-
dences thereof. Stool samples were taken and tested regard-
ing the level of calprotectin, and the eye examination
consisted of the slit-lamp exam, tonometry, visual acuity,
and indirect ophthalmoscopy.
Ethics and Consent
The present study was approved by the institutional Ethics
Committee, and permission was obtained from all depart-
ment heads, who were assured that confidentiality would be
maintained and ethical principles would be followed. Before
the beginning of the study, a background about it and the
reason for it were explained, and the targeted population
were encouraged to participate without any undue pressure,
and written informed consent was be obtained.
Statistical Analyses
Sorting and the analysis of the data were performed the using
Statistical Package for Social Sciences (SPSS, IBM Corp.,
Armonk, NY, US), version 21. In this study the qualitative
square test was used for analysis (Mont Carlo exact test and
Fishers exact test were used as alternatives for Chi-square
test if there were many small expected values). Numerical
variables were expressed as mean
standard deviation or
median (IQR). The independent sample t-test (for normal
distributed data) or Mann-Whitney U-test (for non-normal
distributed data) were used for comparison between groups.
P value ( 0.05) was adopted as the level of significance.
Results
A total of 120 patients with IBD were enrolled in the present
study.
►Table 1 shows the demographics of the sample, which
was composed of 52 (43.3%) male patients and 68 (56.7%)
were female patients whose mean age was 35.5
13.3 years.
Ocular affections represent  22.5% of EIMs; other EIMs
were observed in 41 (34.1%) patients in the sample: in 29.9%
of those with ulcerative colitis, and in 52% of those with
Crohn disease (►Table 2). The incidence of EIMs such as
associated systemic lupus erythematosus (SLE), hypothy-
roidism and mullerin agenesis did not exceed 0.8% (one
case for each diagnosis).
There were no statistically significant differences in the
presence of ocular involvement in relation to the Montreal
classification of two types of IBD (ulcerative colitis:
p ¼ 0.269; Crohn disease: p ¼ 1.00; ►Table 3).
►Table 4 shows a comparison of the median level of
calprotectin in relation to the presence of ocular involvement
in the two types of IBD, with no statistically significant
difference (ulcerative colitis: p ¼ 0.562; Crohn disease:
p ¼ 0.968).
The most common ocular findings were conjunctivitis: in
31 cases (25.8%), anterior uveitis in 13(10.8%), scleritis in 11
(9.2%), cataract in 10 (8.3%), posterior uveitis in 4 (3.45%),

Table 1 Demographic characteristics of patients with inflammatory bowel disease who underwent an ophthalmologic
examination

Characteristic Total (n ¼ 120) Ulcerative colitis (n ¼ 97) Crohn disease (n ¼ 23) p-value
Age (years) mean
35.5
13.3 36.3
13.8 32
10.8 .107
standard deviation
Gender – n (%) .020
Male 52 (43.3) 47 (48.5) 5 (21.7)
Female 68 (56.7) 50 (51.5) 18 (78.3)
Other extraintestinal .542
manifestations – n (%)
Hypothyroidism 1 (0.8) 1 (1.0) 0 (0.0)
Mullerin agenesis 1 (0.8) 0 (0.0) 1 (4.3)
Systemic lupus 1 (0.8) 1 (1.0) 0 (0.0)
erythematosus
Patients with ocular 27 (22.5) 23 (23.7) 4 (17.4) .514
manifestations – n (%)

Note: Statistically significant value.

J Coloproctol Vol. 41 No. 1/2021 © 2021. Sociedade Brasileira de Coloproctologia. All rights reserved.
 Ocular Affectation in cases of IBD Ahmed et al. 11

Table 2 Distribution of extraintestinal manifestations

Axial Cut. Erythema Musculo- Perianal PSC Pyoderma Musculoskeletal Renal

arthralgia Fistula nodosum skeletal fistula pyoderma stone
Ulcerative 0 (0.0%) 0 (0.0%) 9 (9.3%) 7 (7.2%) 0 (0.0%) 4 (4.1%) 4 (4.1%) 0 (0.0%) 5 (5.2%)
colitis – n (%)
Crohn 1 (4.3%) 3 (13.0%) 2 (8.7%) 3 (13.0%) 1 (4.3%) 0 (0.0%) 0 (0.0%) 2 (8.7%) 0 (0.0%)
disease – n (%)
Total – n (%) 1 (0.8%) 3 (2.5%) 11 (9.2%) 10 (8.3%) 1 (0.8%) 4 (3.3%) 4 (3.3%) 2 (1.7%) 5 (4.2%)

Table 3 Incidence of ocular involvement in cases of ulcerative colitis and Crohn disease

Ocular involvement – n (%) p-value

Ulcerative colitis E1 (n ¼ 26) 9 (34.6) .269
E2 (n ¼ 46) 10 (21.7)
E3 (n ¼ 25) 4 (16.0)
Total (n ¼ 97) 23 (23.7)
Crohn disease A1L3B1 (n ¼ 13) 2 (15.4) 1.00
A2L3B2 (n ¼ 10) 2 (20.0)
Total (n ¼ 23) 4 (17.4)

reviations: E1, extension limited to the rectum; E2, Left sided UC (distal UC); E3, Extensive UC; A1, age of diagnosis ¼ 16 years or younger; A2 and A3,
age of diagnosis at 17–40 years and >40 years, respectively; L3, ileocolonic; B1, non-stricturing, non-penetrating; B2, stricturing.

Table 4 Median level of calprotectin in relation to the presence or absence of ocular involvement

Level of calprotectin p-value

Median (IQR)
Ulcerative colitis With ocular involvement: 800(528.50-997.25); 0.458
without ocular involvement: 685 (500-913)
Crohn disease With ocular involvement: 750(133.25-2462.50); 0.785
without ocular involvement: 1000(320-1500)

Fig. 1 Ocular manifestation on patient with inflammatory bowel disease.

J Coloproctol Vol. 41 No. 1/2021 © 2021. Sociedade Brasileira de Coloproctologia. All rights reserved.
12 Ocular Affectation in cases of IBD Ahmed et al.

Discussion

The ocular complications of IBD are still a problematic issue

Fig. 2 Recurrent anterior uveitis with secondary intraocular lens after
complicated cataract.
not only in Egypt; they are an ongoing worldwide challenge,
due to their early onset and silent progressive course. In the
present study, EIMs were in 41 (34.1%) patients: in 29.9% of
those with ulcerative colitis, and in 52% of those with Crohn
disease. Peyrin-Biroulet et al4 stated that the prevalence of
EIMs is variable, and it ranges between 12% and 35% in cases
of ulcerative colitis, and between 25% and 70% in cases of
Crohn disease. In the present study, dermatological and
musculoskeletal manifestations are the second most com-
mon after ocular affections, a result which is in line with the
one reported by the guidelines of the Brazilian Study Group
of Inflammatory Bowel Diseases.7
The eyes are involved in about 22.5% of all EIMs; never-
theless Felekis et al.,8 in a prospective study, performed
complete eye examinations in 60 IBD patients, and found a
frequency of 43% of ocular EIMs. However, this higher
percentage could be due to the inclusion of patients with
previous chronic eye diseases.
In their study, Akpek et al.6 stated that ocular involvement
does not always coincide with an active intestinal flare. In the
present study, we observed no statistically significant differ-
ences in the presence of ocular involvement in relation to the
Montreal classification of two types of IBD (ulcerative colitis:
p ¼ 0.269; Crohn disease: p ¼ 1.00), or regarding the mean
level of calprotectin.
Different incidence rates of ocular EIMs have been reported
in previous studies8,9; in the present study, the most common
ocular findings were conjunctivitis: in 31 cases (25.8%), ante-
rior uveitis in 13(10.8%), scleritis in 11 (9.2%), cataract in 10
(8.3%), posterior uveitis in 4 (3.45%), and 3 cases in glaucoma
(2.5%) with no statistically significant differences between
ulcerative colitis and Crohn disease. In another study, Petrelli
et al.,9 stated that the prevalence of ocular complications
observed in cases of IBD varies among studies (uveitis:
0.0001% to 0.01%; conjunctivitis: 0.1% to 7%; blepharitis:
3.5% to 15%; and cataract: 0.3% to 15%).
The present study has several limitations, such as the
relatively small sample size and no addressing of correlation
between laboratory findings and the severity of eye affection.

Conclusion
Ocular manifestations among IBD patients are common and
usually nonspecific in their presentation; therefore, eye
examinations should be a part of the routine assessment
and follow-up of IBD patients. The early diagnosis and man-
agement of ocular EIMs may prevent serious complications
that could be associated with significant visual deterioration.
In addition, the general practitioner and gastroenterologist
Fig. 3 Conjunctivitis, scleritis and episcleritis.
should be aware of the frequency and variety of EIMs in
general, such as uveitis and sclerites, for they might precede
a diagnosis of ulcerative colitis or Crohn disease.
and 3 cases in glaucoma (2.5%), with no statistically signifi-
cant difference between ulcerative colitis and Crohn disease Conflict of Interests
(►Fig. 1-3). The authors have no conflict of interests to declare.

J Coloproctol Vol. 41 No. 1/2021 © 2021. Sociedade Brasileira de Coloproctologia. All rights reserved.

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